Objectives To undertake the first comprehensive analysis of the incidence of three curable sexually transmissible infections (STIs) within remote Australian Aboriginal populations and provide a basis for developing new control initiatives.
Methods We obtained all results for Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG) and Trichomonas vaginalis (TV) testing conducted during 2009–2011 in individuals aged ≥16 years attending 65 primary health services across central and northern Australia. Baseline prevalence and incidence of all three infections was calculated by sex and age group.
Results A total of 17 849 individuals were tested over 35 months. Baseline prevalence was 11.1%, 9.5% and 17.6% for CT, NG and TV, respectively. During the study period, 7171, 7439 and 4946 initially negative individuals had a repeat test for CT, NG and TV, respectively; these were followed for 6852, 6981 and 6621 person-years and 651 CT, 609 NG and 486 TV incident cases were detected. Incidence of all three STIs was highest in 16-year-olds to 19-year-olds compared with 35+ year olds (incident rate ratio: CT 10.9; NG 11.9; TV 2.5). In the youngest age group there were 23.4 new CT infections per 100 person-years for men and 29.2 for women; and 26.1 and 23.4 new NG infections per 100 person-years in men and women, respectively. TV incidence in this age group for women was also high, at 19.8 per 100 person-years but was much lower in men at 3.6 per 100 person-years.
Conclusions This study, the largest ever reported on the age and sex specific incidence of any one of these three curable infections, has identified extremely high rates of new infection in young people. Sexual health is a priority for remote communities, but will clearly need new approaches, at least intensification of existing approaches, if a reduction in rates is to be achieved.
- CHLAMYDIA TRACHOMATIS
- NEISSERIA GONORRHOEA
- EPIDEMIOLOGY (CLINICAL)
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Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG) and Trichomonas vaginalis (TV) are sexually transmissible infections (STIs) of the genital tract that can lead to serious reproductive complications and other adverse outcomes.1 ,2 These STIs are usually asymptomatic and often remain untreated and infectious. Despite the availability for many years of curative, single dose therapy, high prevalence of infection have been sustained in many populations.3 For over two decades, all three infections have been reported to occur at higher levels among Aboriginal and Torres Strait Islander (hereafter referred to as ‘Aboriginal’) people in Australia compared with non-Aboriginal populations,4 within geographically remote communities in central and northern regions. In 2012, CT and NG notification rates in the Aboriginal population residing in remote communities were 2897 and 2384 per 100 000 people, respectively, just over 8 and 40 times higher than the Australian population.5 For TV, prevalence studies based on clinic attendees suggest rates 50-fold greater in women in remote Aboriginal communities compared with urban areas.6 ,7 The introduction of nucleic acid based diagnostic tests in Australia led to the implementation of screening programmes for these infections in a number of remote communities. However, despite a few notable local successes,8 substantial and sustained reductions in prevalence have not generally occurred.
A central public health question on the control of curable STIs is how often those at risk should be offered screening and treatment. The answer to this question depends on the rate at which new infections occur and requires population-based information on the incidence of infection. However, incidence, which is also a key indicator of the effectiveness of STI prevention strategies, has been notoriously hard to measure reliably, because it requires accurate, repeat screening of large and representative samples of the population. Internationally, most studies reporting incidence are from clinical trials for the prevention of STIs9 or highly select cohorts10 or clinic attendees.11 ,12 Incidence studies conducted in the general population have generally been small-scale and reporting CT incidence in women only.13 ,14 There is a lack of large-scale studies reporting on the incidence of curable STIs in the general population.
In 2010, a cluster randomised trial15 of health service strategies for improving the control of curable STIs was initiated in 68 remote Aboriginal communities in central and northern Australia. In the context of this trial, it became possible for the first time to obtain records of repeat screening for STIs in these communities, and therefore estimate the rate at which new infections were occurring. We report here on the baseline prevalence and incidence of STIs in the trial population.
We conducted a retrospective cohort analysis, making use of baseline data collected in the context of STRIVE15 (STIs in remote communities: Improved and enhanced primary health care). The STRIVE trial aimed to evaluate quality improvement strategies in the clinical management of STIs. These communities have predominantly (>90%) Aboriginal residents and range in size from approximately 200 to 2500 residents. They are located in four geographical regions: 28 in Central Australia and 29 in the ‘Top End’ of the Northern Territory, eight in the Kimberley region of Western Australia and three in the Cape York region of Queensland. Participating health services follow regional clinical guidelines,16–19 established before the trial began, that recommend screening for CT and NG through collection of urine from men, and self-collected vaginal swabs or urine from women. For TV, guidelines varied among jurisdictions, with screening recommended for both men and women in the Northern Territory and for women only in ‘endemic areas’ of Western Australia and Queensland. The age group targeted for screening also varied across jurisdictions but generally referred to sexually active people aged <40 years. Frequency of screening was not specified explicitly in all guidelines at the time the data were collected, but was broadly accepted to be annual19 ,20 and is recommended in current guidelines.
Communities involved in STRIVE each have only one clinical service provider, each of which is served by one of three pathology laboratories (depending on region) that test specimens for CT, NG and TV using nucleic acid amplification tests. All three laboratories comply with Australian national pathology accreditation standards and have stringent controls on the quality of specimen handling and testing, and the reporting back of results to clinical services. For the analyses reported in this paper, we obtained a complete data set of de-identified line records from these laboratories on all CT, NG and TV testing in people aged 16 years or more that took place at 65 of the 68 participating STRIVE sites during the period from 1 January 2009 to 31 October 2011. For each test, the line record contained information on age, sex, date of test, result and where the test took place. A unique identifier (in coded form) was also provided to link multiple tests by an individual within the same health service. We were unable to link across different health services.
The STRIVE trial, including the baseline data collection and analysis reported here, was approved by all relevant bodies responsible for ethical review of health research as per the STRIVE protocol.15
Analyses reported in this paper were restricted to STI tests recorded as conducted at one of the participating health services, in people 16 years or older at the time of testing. We calculated STI positivity at first test during the study period, by dividing the number of unique individuals whose first test in the period was positive, by the number of individuals tested, stratified by sex and 5 year age groups.
An incident infection of each type (CT, NG, TV) was defined as a record of a positive test result in a person whose first test was negative. Treatment data were not available from the laboratory records, so in order to create a negative cohort for each infection to calculate incidence, all individuals whose first test in the study period was positive were excluded from the incidence analyses for each infection type. Calculation of incidence for each infection type was based on individuals with a record of at least two tests for that infection in the study period and calculated as the number of incident infections divided by the person-years of follow-up. We estimated the date of infection as the midpoint between the last negative test and first positive test for each infection type (CT, NG, TV), at which point follow-up ceased (i.e. was censored) for the purpose of incidence calculation. For those who did not acquire infection, the follow-up time was the difference between the dates of last and first negative tests. We calculated the rate of incident infection and associated 95% CIs using the person-years method.
Incidence rates were stratified by age group, sex and whether a different STI preceded or concurred with the incident infection. Finally, we calculated incidence rate ratios (IRR) with 95% CIs using random effects Poisson regression methods to take into account within-person variation for repeat testers. SAS statistical software V.9.1.321 was used to conduct all analyses. A cut-off of p<0.05 was used to define statistical significance.
Over the 35-month study period, 17 849individuals had at least one test result recorded for one of the three STIs. Women made up a higher proportion than men of those tested (CT 58%; NG 58%; TV 63%). The median age of all individuals at first test was 30 years (IQR 22–40). Of those individuals aged ≥35 years, 75% were aged <49 years.
Prevalence of infection
Of 17 848 individuals tested for CT, 1989 (11.1%) had a positive first test during the study period. Overall CT prevalence was higher in women than men (12.1% versus 9.7%, p<0.01) and greatest in the age group 16–19 years for women (26.5%) and men (20.5%) (see online supplement 1). Of 17 773 individuals tested for NG, 1693 (9.5%) had a positive first test, with prevalence higher in men than women (10.4% versus 8.9%, p<0.01) and greatest in the age group 16–19 years for men (21.6%) and women (20.1%) (see online supplement 1). Of 13 502 individuals tested for TV, 2371 (17.6%) had a positive first test, with women 3.6 times more likely to do so than men (23.9% versus 6.7%, p<0.01) (see online supplement 1). In women, TV prevalence was also highest (31.5%) in the age group 16–19 years whereas in men, prevalence was highest in people aged 35 years or more (7.8%). In contrast to prevalence for CT and NG, which declined rapidly with age in men and women, prevalence for TV remained steady across all age groups in men (range: 5.6%–7.8%) and declined slightly with age in women (31.5%–20.2%). Prevalence for each infection varied across the four regions over a roughly twofold range for CT (7.1%–13.6% in men and 7.5%–18.9% in women); a threefold range for NG (5.6%–17.4% in men and 5.9%–15.3% in women). TV prevalence spanned a threefold range in men (2.6–7.9%) but was more evenly distributed across regions in women (19.7%–28.3%).
Incidence of infection
Around 40% of men and over half the women had two or more tests for at least one of the infections during the study period (see online supplement 2). The proportion with repeat tests decreased with age for men (from 44% in 16-year-olds to 19- year-olds to 34% in 35+ year olds) and women (from 60% in 16-year-olds to 19-year-olds to 45% in 35+ year olds) (p<0.001) (see online supplement 2). There were 7171 individuals negative for CT at first test who had a second test during the study period. In 6852 person-years of follow-up, there were 651 incident cases giving an overall CT incidence rate of 9.5 per 100 person-years (table 1). Similarly, for 7439 individuals negative for NG (table 2) and 4946 individuals negative for TV (table 3), there were 609 and 486 incident cases, giving overall incidence rates of 8.7 and 7.3 per 100 person-years, respectively. People with a prevalent TV or NG infection were more likely to have an incident CT infection (table 1). The incidence of CT did not differ by sex (IRR 1.06, p=0.565) but for NG it was significantly less in women (IRR 0.67, p≤0.001) while for TV it was significantly higher in women (IRR 4.39, p≤0.001). The incidence of all three infections was highest in 16-year-olds to 19-year-olds, at 23.4 and 29.2 per 100 person-years for CT in men and women, respectively (table 1); 26.1 and 23.4 for NG (table 2) and 3.6 and 19.8 for TV (table 3). Incidence fell sharply with age for both CT and NG, but more gradually for TV, as shown in figure 1.
To our knowledge, this is the largest study ever conducted of the incidence of all three common, curable STIs in women and the only study of all three STIs in both men and women. Our study provides new knowledge on the contrasting epidemiology of these infections. It is also the first analysis of TV incidence in both men and women within the same population,13 ,14 ,22 and the first in both sexes to be based on highly sensitive and specific nucleic acid detection, as opposed to the older culture or microscopy methods. Accurately defining the incidence of infection in addition to the prevalence provides insight into the duration of infection,23 a key parameter in determining the frequency of screening needed to reduce rates of infection and thereby the burden of disease.
There are a number of methodological issues that need to be considered when interpreting these data. First, the screening reported was based on routine clinical activity and did not aim to include all individuals residing in participating communities. However, screening is likely to have covered a large proportion of the population, as the number of individuals recorded as tested during the period actually exceeds the best available population estimates for these communities.24 Second, we made analytical decisions in regard to selection of tests and any censoring that may have influenced outcomes. We excluded the substantial group (CT 15%, NG 12%, TV 27%) of people whose first test in the study period was positive because we could not be sure that they had been treated and, therefore, confirm their eligibility for follow-up to detect a new infection. In other incidence studies,13 a history of a positive test has been predictive of a new infection, so it is possible that this exclusion led to a downward bias in incidence rates in our study. Similarly, by censoring at the estimated date of acquisition, we may have missed subsequent new infections occurring in people who were treated, again possibly resulting in underestimation of incidence.
Censoring is an important consideration, especially given our reliance on laboratory data alone to calculate incidence. Based on available natural history studies,25 the 34-month study period was longer than the mean duration of untreated CT and NG, so it is possible that incident infections occurred but cleared spontaneously before the second test; this would again lead to incidence being underestimated. Urethral TV in men is considered to be most often asymptomatic and have high rates of spontaneous clearance,26 consistent with our finding of a substantially lower incidence of TV in men than in women. In contrast, NG in men is commonly symptomatic and may be expected to lead to treatment seeking, and a recorded test. CT, while commonly asymptomatic, lasts longer than untreated TV in men.25 Analytically, we could have addressed the issue of spontaneous clearance by restricting follow-up for each individual to 1 year (for example), but this strategy may have resulted in upward bias in incidence estimates.
Faced with these analytical options, and given the widespread perception that rates of STIs are high in remote Aboriginal populations, we preferred to use strategies that were likely to err in the direction of underestimating rather than overestimating incidence. There is, nevertheless, still potential for over-representation of those at higher risk, if those in the study population who were negative for infection and subsequently retested during the study period were at higher risk than other members of the community. Finally, we were unable to link records across clinics, so cannot exclude the possibility that some individuals re-entered the analysis through attendance at multiple services.
Despite these limitations, our study provides the first comprehensive set of age and sex specific prevalence and incidence estimates of all three infections in the same study population. There have been similar findings of high STI prevalence in Canada's First Nations people and Native Americans in the USA.27 ,28 The only previously reported incidence study in any Aboriginal or First Nations population was based on much smaller numbers of 1034 people22 and did not report on TV. This study,22 from a remote Aboriginal population in 1998, found the overall incidence of CT to be almost 50% higher than the rate we found and NG over twice the rate. However, this study was conducted in only one of the four geographical regions of our study, which may explain the difference. The one general population study13 of STI incidence in Australia reported only on CT in urban, mainly non-Aboriginal women, and found rates four times lower in the age group 16–19 years than seen in our study. Incidence estimates of a comparable magnitude with those reported here have been seen exclusively in populations selected on the basis of high risk.10
Our study is the first to report on TV incidence by sex and age. Earlier studies have been mostly limited to women, who are either pregnant, adolescents or STI clinic attendees12 ,29 and only one used PCR.29 In contrast to previous studies, we found that both TV prevalence (estimated by positivity rates) and incidence in women was highest in the younger age groups (table 3) and both declined with increasing age. Earlier prevalence studies conducted internationally, including one7 in 1996 among Aboriginal women in Australia found that prevalence increased with age and was highest in women over 35 years. A subsequent study30 in 2001 among Aboriginal women found that prevalence decreased with age, a finding replicated in our analysis. One possible explanation is that routine screening for TV, introduced during the late 1990s in many Aboriginal communities, has lowered the prevalence of TV in the older women but among younger women, who have a higher incidence, prevalence has been sustained through reinfection.
The implications of our findings are that if the burden of these three curable STIs is to be reduced substantially through screening and treatment, the duration of infection will need to be shortened through encouraging those at the highest risk, particularly in the youngest age groups, to be tested more frequently than is currently occurring. Our study found that the high prevalence of CT and NG was matched by a similarly high incidence, indicating that the average duration of these infections (prevalence divided by the incidence) is about 1 year in men and women, suggesting that more frequent, perhaps 6 monthly, screening may be required. Only for TV the substantially higher prevalence compared with incidence suggests that yearly screening may be adequate. Ideally, screening should occur as soon after infection as possible to ensure that the risk of transmission is minimised.
Given the very much higher incidence of these infections in people aged 16–19 years, strategies to increase screening that are focused on this age group is going to be critical to success. Possible options to investigate further, that may lead to more frequent screening, include removing barriers to patients accessing services, such as concerns about confidentiality, ensuring the availability of gender-specific staff and offering outreach-based screening. Improving public health education about the importance of regular STI screening, identifying at-risk behaviour and recognising symptoms may also lead to more frequent screening among young people.
We have demonstrated the feasibility and utility of analysing STI incidence from routine clinical records to track the occurrence of infection in a highly endemic setting. It is likely that a new approach, or at least a genuine intensification of existing approaches, will be required to generate a long-term reduction in the occurrence of these infections and their complications.
This study provides the first comprehensive set of age and sex specific incidence estimates of Chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis in any population.
This study also provides the first estimate of trichomoniasis incidence in men and women in the same population.
Our study found extreme incidence of all three sexually transmissible infections (STIs) in the youngest age group (16–19 years).
Findings suggest that to reduce this burden of curable STIs, young people in remote Australian Aboriginal communities need to be tested more frequently.
Correction notice This article has been corrected since it was published Online First. The Contributors statement has been amended.
Handling editor Jackie A Cassell
Acknowledgements STRIVE is a collaboration between researchers named in the authorship list, conducted in partnership with the Northern Territory Department of Health, the Aboriginal Medical Services Alliance of the Northern Territory, Apunipima Cape York Health Council, Kimberley Aboriginal Medical Services Council and the Western Australia Country Health Service. The study would not have been possible without the commitment of all participating health services and their staff and the ongoing support and advice from our partners. The authors acknowledge the important contributions of the STRIVE Executive Committee. The authors are grateful to Western Diagnostic Pathology, Pathwest Laboratory Medicine WA, SA Pathology and Queensland Health Pathology and Scientific Services, and their staff that undertook testing for STIs on behalf of participating health services, and provided the anonymous line record data that formed the basis for the analyses reported here.
Collaborators Additional STRIVE Investigators (not named as authors): Donna Ah Chee, John Boffa, David Glance, Mathew Law, Robyn McDermott and Steven Skov.
Contributors JMK, JW, RJG, AR, SM, BJS, LG, BH and DTT developed the STRIVE study protocol which led to the current data set being available. RJG conceived the idea for this analysis. JMK, HW, RJG, BJS were responsible for the study design and planning for this analysis. BJS did the literature search. HW did the primary data analysis. BJS and RJG wrote the first draft. LG, BH, JK, BJS, DTT were involved in study implementation and field data collection, and SM and AD were involved in overall data management and analysis. All authors reviewed and revised drafts, contributed to the interpretation of the results and read and approved the final manuscript. BJS prepared the final manuscript and processed the submission.
Funding Australian National Health and Medical Research Council (NHMRC), Project Grant ID: 568806. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The views expressed in this publication are those of the authors and do not reflect the views of NHMRC. JMK, RJG, ARR, BD and LM are supported by NHMRC fellowships.
Competing interests None.
Ethics approval Central Australian Human Research Ethics Committee, the Human Research Ethics Committee of the Northern Territory Department of Health and Families and Menzies School of Health Research, Cairns and Hinterland Health Service District Human Research Ethics Committee, Western Australian Country Health Service Board Research Ethics Committee, Western Australian Aboriginal Health Information and Ethics Committee and the University of New South Wales Human Research Ethics Committee.
Provenance and peer review Not commissioned; externally peer reviewed.